Style head in Apocynaceae: a very complex secretory activity performed by one tissue

Submitted: 20 March 2024
Accepted: 25 March 2024
Published: 2 April 2024
Abstract Views: 89
PDF: 69
HTML: 0
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

Nuptial glands are very diverse and associated with different pollination mechanisms. The greater the specificity in the pollen transfer mechanism from anther to stigma, the greater the morphological elaboration of flowers and functional complexity of the nuptial glands. In Apocynaceae, pollination mechanisms reached an extreme specificity, a fact that was only possible due to an extreme morphological synorganization and a profusion of floral glands. Although these glands are of different types, the vast majority have secretory cells only in the epidermis. In general, these epidermal cells produce many different compounds at the same time, and previous studies have demonstrated that in the style head, the functional complexity of epidermis has become even greater. Four types of style head are found in the family, which have different degrees of functional complexity in relation to the secretion produced and pollen dispersal mechanism. The secretion is fluid in types I, II and III, and the pollen is dispersed and adhered to the pollinator by the secretion produced by the style head. In type IV, the secretion hardens and acquires a specific shape, moulded by the spatial constraints of the adjacent floral organs. This evolutionary alteration is accompanied by changes in the structure and arrangement of the secretory cells, as well as in pollen aggregation and position of stigma. Histochemical analysis has shown that the secretion is mixed and highly complex, especially in the style head type IV, where the secretion, called translator, is formed by a rigid central portion, which adheres to the pollinator, and two caudicles that attach to two pollinia. The translator has a distinct composition in its different parts. Further studies are needed to answer the new questions that have arisen from the discovery of this highly functional complexity of the secretory tissue.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Coiffard C, Gomez B, Daviero-Gomez V, Dilcher DL. Rise to dominance of angiosperm pioneers in European Cretaceous environments. Proc Natl Acad Sci USA 2012;109:20955-9. DOI: https://doi.org/10.1073/pnas.1218633110
Stebbins GL. Why are there so many species of flowering plants? Bioscience 1981;31:573-7. DOI: https://doi.org/10.2307/1308219
Midgley JJ, Bond WJ. How important is biotic pollination and dispersal to the success of the angiosperms? Philos T Roy Soc B 1991;333:209-15. DOI: https://doi.org/10.1098/rstb.1991.0069
Berendse F, Scheffer M. The angiosperm radiation revisited, an ecological explanation for Darwin’s “abominable mystery”. Ecol Lett 2009;12:865-72. DOI: https://doi.org/10.1111/j.1461-0248.2009.01342.x
Nicolson SW, Nepi M, Pacini E. Nectaries and nectar. Springer, Dordrecht; 2007. DOI: https://doi.org/10.1007/978-1-4020-5937-7
Tölke ED, Capelli NV, Pastori T, Alencar AC, Cole TCH, Demarco D. Diversity of floral glands and their secretions in pollinator attraction. In: Mérillon JM, Ramawat KG, Editors. Coevolution of secondary metabolites. Reference Series in Phytochemistry. Springer, Cham 2019; p. 1-46. DOI: https://doi.org/10.1007/978-3-319-76887-8_48-3
Sponsler D, Iverson A, Steffan-Dewenter I. Pollinator competition and the structure of floral resources. Ecography 2023;2023:e06651. DOI: https://doi.org/10.1111/ecog.06651
Vogel S. The role of scent glands in pollination. On the structure and function of osmophores. Translated by J.S. Bhatti, Amerind Publishing, New Delhi; 1990.
Armbruster WS. The role of resin in angiosperm pollination: ecological and chemical considerations. Am J Bot 1984;71:1149-60. DOI: https://doi.org/10.1002/j.1537-2197.1984.tb11968.x
Boff S, Demarco D, Marchi P, Alves-dos-Santos I. Perfume production in flowers of Angelonia salicariifolia attracts males of Euglossa annectans which do not promote pollination. Apidologie 2015;46:84-91. DOI: https://doi.org/10.1007/s13592-014-0305-2
Lunau K, Wester P. Mimicry and deception in pollination. Adv Bot Res 2017;82:259-79. DOI: https://doi.org/10.1016/bs.abr.2016.10.005
Demarco D. Floral glands in asclepiads: structure, diversity and evolution. Acta Bot Bras 2017;31:477-502. DOI: https://doi.org/10.1590/0102-33062016abb0432
Tilton VR, Horner HT Jr. Stigma, style, and obturator of Ornithogalum caudatum (Liliaceae) and their function in the reproductive process. Am J Bot 1980;67:1113-31. DOI: https://doi.org/10.1002/j.1537-2197.1980.tb07744.x
Endress PK. Development and evolution of extreme synorganization in angiosperm flowers and diversity: a comparison of Apocynaceae and Orchidaceae. Ann Bot 2016;117:749-67. DOI: https://doi.org/10.1093/aob/mcv119
Demarco D. Secretory tissues and the morphogenesis and histochemistry of pollinarium in flowers of Asclepiadeae (Apocynaceae). Int J Plant Sci 2014;175:1042-53. DOI: https://doi.org/10.1086/677947
Demarco D. Staminal wing gland: a novel secretory structure of asclepiads. Botany 2017;95:763-72. DOI: https://doi.org/10.1139/cjb-2016-0239
Monteiro MM, Demarco D. Corona development and the floral nectaries in Asclepiadeae (Asclepiadoideae, Apocynaceae). Acta Bot Bras 2017;31:420-32. DOI: https://doi.org/10.1590/0102-33062016abb0424
Ribeiro JC, Ferreira MJP, Demarco D. Colleters in Asclepiadoideae (Apocynaceae): protection of meristems against desiccation and new functions assigned. Int J Plant Sci 2017;178:465-77. DOI: https://doi.org/10.1086/692295
Medina MC, Sousa-Baena MS, Capelli NV, Koch R, Demarco D. Stinging trichomes in Apocynaceae and their evolution in angiosperms. Plants 2021;10:2324. DOI: https://doi.org/10.3390/plants10112324
Wyatt R, Lipow SR. A new explanation for the evolution of pollinia and loss of carpel fusion in Asclepias and the Apocynaceae s.l. Ann Mo Bot Gard 2007;94:474-84. DOI: https://doi.org/10.3417/0026-6493(2007)94[474:ANEFTE]2.0.CO;2
Ollerton J, Liede-Schumann S, Endress ME, Meve U, Rech AR, Shuttleworth A. et al. The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study. Ann Bot 2019;123:311-25. DOI: https://doi.org/10.1093/aob/mcy127
Bitencourt C, Nürk NM, Rapini A, Fishbein M, Simões AO, Middleton DJ. et al. Evolution of dispersal, habit, and pollination in Africa pushed Apocynaceae diversification after the Eocene-Oligocene climate transition. Front Ecol Evol 2021;9:719741. DOI: https://doi.org/10.3389/fevo.2021.719741
Fallen ME. Floral structure in the Apocynaceae: morphological, functional and evolutionary aspects. Bot Jahrb Syst 1986;106:245-86.
Endress ME, Bruyns PV. A revised classification of Apocynaceae s.l. Bot Rev 2000;66:1-56. DOI: https://doi.org/10.1007/BF02857781
Endress PK. Diversity and evolutionary biology of tropical flowers. University Press, Cambridge; 1994.
Demarco D. [Glândulas de órgãos vegetativos aéreos e florais de espécies de Asclepiadeae (R.Br.) Duby (Asclepiadoideae, Apocynaceae) de Mata Atlântica do Estado de São Paulo].[PhD dissertation in Portuguese]. Universidade Estadual de Campinas; 2008.
Endress PK, Jenny M, Fallen ME. Convergent elaboration of apocarpous gynoecia in higher advanced dicotyledons (Sapindales, Malvales, Gentianales). Nord J Bot 1983;3:293-300. DOI: https://doi.org/10.1111/j.1756-1051.1983.tb01941.x
Walker DB. Postgenital carpel fusion in Catharanthus roseus (Apocynaceae). I. Light and scanning electron microscopic study of gynoecial ontogeny. Am J Bot 1975;64:457-67. DOI: https://doi.org/10.1002/j.1537-2197.1975.tb14070.x
Demarco D. [Estruturas secretoras florais e coléteres foliares em espécies de cerrado de Aspidosperma Mart. e Blepharodon Decne. (Apocynaceae s.l.)].[Master’s thesis in Portuguese]. Universidade Estadual de Campinas; 2005.
Kunze H. Structure and function in asclepiad pollination. Plant Syst Evol 1991;176:227-53. DOI: https://doi.org/10.1007/BF00937909
Fishbein M, Livshultz T, Straub SCK, Simões AO, Boutte J, McDonnell A, Foote A. Evolution on the backbone: Apocynaceae phylogenomics and new perspectives on growth forms, flowers, and fruits. Am J Bot 2018;105:495-513. DOI: https://doi.org/10.1002/ajb2.1067
Swarupanandan K, Mangaly JK, Sonny TK, Kishorekumar K, Chand Basha S. The subfamilial and tribal classification of the family Asclepiadaceae. Bot J Linn Soc 1996;120:327-69. DOI: https://doi.org/10.1111/j.1095-8339.1996.tb00486.x
Kunze H. Evolution of the translator in Periplocaceae and Asclepiadaceae. Plant Syst Evol 1993;185:99-122. DOI: https://doi.org/10.1007/BF00937723
Kunze H. Ontogeny of the translator in Asclepiadaceae s.str. Plant Syst Evol 1994;193:223-42. DOI: https://doi.org/10.1007/BF00983552
Kunze H. Floral morphology of some Gonolobeae (Asclepiadaceae). Bot Jahrb Syst 1995;117:211-38.
Rapini A, van den Berg C, Liede-Schumann S. Diversification of Asclepiadoideae (Apocynaceae) in the New World. Ann Mo Bot Gard 2007;94:407-22. DOI: https://doi.org/10.3417/0026-6493(2007)94[407:DOAAIT]2.0.CO;2
Endress ME, Meve U, Middleton DJ, Liede-Schumann S. Apocynaceae. In: Kadereit J, Bittrich V, Editors. Flowering plants. Eudicots. The families and genera of vascular plants. Springer, Cham 2018; p. 207-411. DOI: https://doi.org/10.1007/978-3-319-93605-5_3
Livshultz T, Hochleitner S, Lakata E. Pollen transfer efficiency of Apocynum cannabinum (Apocynaceae): a comparative perspective. J Poll Ecol 2018;22:35-48. DOI: https://doi.org/10.26786/1920-7603(2018)four
Nilsson S, Endress ME, Grafström E. On the relationship of the Apocynaceae and Periplocaceae. Grana 1993;2:3-20. DOI: https://doi.org/10.1080/00173139309428973
Wiemer AP, Sérsic AN, Marino S, Simões AO, Cocucci AA. Functional morphology and wasp pollination of two South American asclepiads (Asclepiadoideae-Apocynaceae). Ann Bot 2012;109:77-93. DOI: https://doi.org/10.1093/aob/mcr268
Heslop-Harrison Y. Stigma characteristics and angiosperm taxonomy. Nord J Bot 1981;1:401-20. DOI: https://doi.org/10.1111/j.1756-1051.1981.tb00707.x
Woodson RE, Moore JA. The vascular anatomy and comparative morphology of Apocynaceae flowers. Bull Torrey Bot Club 1938;65:135-66. DOI: https://doi.org/10.2307/2481100
Rao VS, Ganguli A. Studies in the floral anatomy of the Apocynaceae. J Indian Bot Soc 1963;42:419-35.
Kunze H, Liede S. Observations on pollination in Sarcostemma (Asclepiadaceae). Plant Syst Evol 1991;178:95-105. DOI: https://doi.org/10.1007/BF00937984
Vieira MF, Shepherd GJ. Oxypetalum banksii subsp. banksii: a taxon of Asclepiadaceae with an extragynoecial compitum. Plant Syst Evol 2002;233:199-206. DOI: https://doi.org/10.1007/s00606-002-0204-2
Demeter K. [Vergleichende Asclepiadeenstudien].[Article in German]. Flora 1922;15:130-76. DOI: https://doi.org/10.1016/S0367-1615(17)31263-6
Safwat FM. The floral morphology of Secamone and the evolution of the pollinating apparatus in Asclepiadaceae. Ann Mo Bot Gard 1962;49:95-129. DOI: https://doi.org/10.2307/2394742
Schnepf E, Witzig F, Schill R. [Über Bildung und Feinstruktur des Translators der Pollinarien von Asclepias curassavica und Gomphocarpus fruticosus (Asclepiadaceae)].[Article in German]. Trop Subtrop Pflanzenwelt 1979;25:1-33.
Vijayaraghavan MR, Cheema K. Ontogenetical and histochemical studies on the translator apparatus in Calotropis procera R.Br. I. The retinaculum. Acta Histochem 1977;59:15-20. DOI: https://doi.org/10.1016/S0065-1281(77)80074-3
Kunze H. Pollination ecology in two species of Gonolobus (Asclepiadaceae). Flora 1999;194:309-16. DOI: https://doi.org/10.1016/S0367-2530(17)30919-2
Johansen DA. Plant microtechnique. McGraw-Hill, New York; 1940.
Lillie RD. Histopathologic technic and practical histochemistry. McGraw-Hill, New York; 1965.
Gerlach D. [Botanish Mikrotechnik: eine Einführung].[Book in German]. Georg Thieme, Stuttgart; 1984.
Pearse AGE. Histochemistry: theoretical and applied. C. Livingstone, Edinburgh; 1985.
Cain AJ. The use of Nile Blue in the examination of lipids. Quart J Microsc Sci 1947;88:383-92. DOI: https://doi.org/10.1242/jcs.s3-88.3.383
Ganter P, Jollès G. [Histochimie normale et pathologique].[Book in French], vol. 1. Gauthier-Villars, Paris; 1969.
Ganter P, Jollès G. [Histochimie normale et pathologique].[Book in French], vol. 2. Gauthier-Villars, Paris; 1970.
Fisher DB. Protein staining of ribboned epon sections for light microscopy. Histochemie 1968;16:92-6. DOI: https://doi.org/10.1007/BF00306214
McManus JFA. Histological and histochemical uses of periodic acid. Stain Technol 1948;23:99-108. DOI: https://doi.org/10.3109/10520294809106232
Gregory M, Baas P. A survey of mucilage cells in vegetative organs of the dicotyledons. Isr J Bot 1989;38:125-74.
Pizzolato TD. Staining of Tilia mucilages with Mayer’s tannic acid-ferric chloride. Bull Torrey Bot Club 1977;104:277-9. DOI: https://doi.org/10.2307/2484311
Demarco D. Histochemical analysis of plant secretory structures. Methods Mol Biol 2023;2566:291-310. DOI: https://doi.org/10.1007/978-1-0716-2675-7_24

Supporting Agencies

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

How to Cite

Maximo, D., & Demarco, D. (2024). Style head in Apocynaceae: a very complex secretory activity performed by one tissue. European Journal of Histochemistry, 68(1). https://doi.org/10.4081/ejh.2024.4027